Evaluation of leaf rust resistance in selected bread wheat accessions from the National Plant Gene Bank of Iran

Document Type : Research Paper

Authors

1 Department of Plant Protection, College of Agriculture & Natural Resources, University of Tehran, Karaj, Iran

2 Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization (AREEO) Karaj, Iran

3 Department of Plant Breeding, College of Agriculture & Natural Resources, University of Tehran, Karaj, Iran

Abstract

The prevalence of wheat leaf rust has increased in recent years due to global climate change conditions. The disease spreads in warm and humid areas in the north and south regions of Iran, causing damage to the susceptible cultivars. Plant germplasms in each country hold rich reserves of resistance genes that influence biotic and abiotic stress. In this study, 100 germplasms of Iranian bread wheat which had previously shown resistance to stem rust, 10 cultivars commonly grown in Iran and two susceptible cultivars, Bolani and Morocco, were selected for greenhouse and field experiments. Greenhouse experiments were conducted to evaluate the performance of a pure isolate from the northern region of the country. The greenhouse experiment followed a completely randomized design, while the field experiment was conducted on the Iraqi-Mahalleh farm in Golestan province using an augmented experimental design. The Bolani and Morocco cultivars showed over 90% infection in the field and 4 scales in the greenhouse. The results indicate that 24.7% of the accessions and cultivars were resistant in both the greenhouse and the field. In addition, 38.1% of the accessions and cultivars were susceptible in the greenhouse but resistant in the field. Conversely, 2.9% were resistant in the greenhouse but, susceptible in the field. Finally, 34.3% exhibited susceptibility in both the greenhouse and the field. The wheat germplasms that were resistant in both conditions and those showing susceptibility in the greenhouse but, resistance in the field were selected for further investigations in developing resistant cultivars.

Keywords


Extended Abstract

Introduction

    Wheat leaf rust, caused by Puccinia triticina, is more prevalent worldwide than the other two wheat rusts. Wheat germplasm held in genebanks is an excellent source of genes for resistance to biotic and abiotic stresses, and Iran, where bread wheat originated, has rich resources of disease resistance genes. Development and production of resistant cultivars is one of the most effective ways of disease management. In this research, the resistance of genetic accession and common cultivars in Iran to leaf rust has been studied.

 

 

Materials and Methods

In this research, resistance to leaf rust was evaluated in 100 purified lines from the bread wheat germplasm collection of the National Plant Gene Bank of Iran and 10 common cultivars in Iran as well as differential lines at both seedling and adult stages. The fungal isolate was collected from the Gorgan region. The isolate was purified by the single postule method, then multiplied and identified. The greenhouse experiments were conducted in the form of a completely randomized design with three replications. The field experiment was conducted in Aragi-Mahaleh station of Gorgan, Golestan province. It was in the form of an augmented design in 5 blocks and replication of 3 cultivars, Araz, Kalate, and Tirgan. Two cultivars, Bolani and Morocco, were used as susceptible cultivars.

 

Results and discussion

The Gor01 isolate's virulence was determined based on its reaction to the differential set. It was found to be virulent on Lr22b, Lr2c, Lr3, Lr3ka, Lr3bg, Lr11, Lr12, Lr13, Lr14a, Lr14b, Lr15, Lr17, Lr22a, Lr23, Lr24, Lr25, Lr29, Lr30, Lr32, Lr33, Lr35, Lr37, Lrb, Lr13 but avirulent on Lr1, Lr2a, Lr2b, Lr9, Lr10, Lr16, Lr18, Lr19, Lr20, Lr21, Lr26, (Lr10, Lr27+ Lr31), Lr28, Lr34. Among the wheat germplasms, 31% were in the susceptible (S) category, 42% were in the moderately susceptible (MS) category, 9% were in the moderately resistant (MR) category and 18% were in the resistant (R) category under greenhouse conditions. Among the varieties, Sarang was in the moderately susceptible category, and Araz and Sirvan were in the moderately resistant category. Two varieties, Bolani and Morocco, were placed in the susceptible category and other varieties were placed in the resistant category. The results of the experiment conducted under field conditions showed that 23% of the wheat germplasm had an S reaction, 16% had an MR reaction, and 3% had an MS reaction; the remaining wheat germplasms also had an R reaction. The Bolani and Morocco cultivars exhibited an S reaction, while the others showed an R reaction.

 

Conclusion

Accessions that had a longer incubation period showed a low infection type. This could be the reaction of the non-race specific gene (genes) for resistance that could phenotypically present the slow rusting reaction. Based on field and greenhouse experiments, it was found that 24.7% of the accessions and cultivars were resistant in both the greenhouse and the field. These accessions could have the all-stage resistant gene(genes) and 38.1% of the germplasms and cultivars were susceptible in the greenhouse but resistant in the field. These germplasms could have the adult plant stage resistant gene(genes). Conversely, only 2.9% showed resistance in the greenhouse but susceptibility in the field reveals the presence of new pathotypes in the field. Finally, 34.3% showed susceptibility in both the greenhouse and the field. The wheat germplasm was resistant in both conditions and those with susceptibility in the greenhouse but resistance in the field were selected for further investigation in the development of resistant cultivars.

ابراهیمیان، مریم؛ نصراله­نژاد­قمی، علی­اصغر؛ زینلی­نژاد، خلیل و رمضانپور، سیده­ساناز (1398). ارزیابی مقاومت به زنگ قهوه ای در مرحله گیاه کامل در تعدادی از ارقام گندم نان. پژوهش‌های تولید گیاهی، 26(3)، 89-102.
اسفندیاری، اسفندیار (1326). زنگ­های غلات در ایران. نشریه آفات و بیماریهای گیاهی،4 ، 76-77 .
افشاری، فرزاد؛ ترابی، محمد؛ کیا، شعبان؛ دادرضایی، سیدطه؛ صفوی، صفرعلی؛ چایچی، مهرداد؛ کربلایی­خیاوی، حسین؛ ذاکری، عبدالکریم؛ بهرامی­کمانگر، سامان؛ نصرالهی، محمود؛ پاتپور، مهران و ابراهیم­نژاد، شاهپور (1384). پایش فاکتورهای بیماریزایی عامل زنگ قهوه­ای گندم (Puccinia triticina Eriksson) در ایران در سال­های 1383-1381. نهال و بذر، 21(4)، 485-496.
بامدادیان،علی ؛ هومند، نوین­چهر؛ حضار، منور و تهرانی، هوشنگ (1370). ارزیابی 27 رقم گندم دارای ژن­های مقاومت به زنگ قهو ه­ا ی گندم در خزانه بین المللی زنگ. مقاله ارایه شده در دهمین کنگره گیاهپزشکی، اهواز، ایران.  ص 113.
ترابی، محمد؛ نظری، کیومرث و افشاری، فرزاد (1380). ژنتیک بیماری زایی Puccinia recondita f. sp. tritici عامل بیماری زنگ قهوه­ای گندم. مجله علوم کشاورزی ایران، 32(3)، 635-625.
دادرضایی، سیدطه و نظری، کیومرث (1394). شناسائی ژن‌های مقاومت به زنگ‌ها درتعدادی از ژنوتیپ‌های گندم ایران با استفاده از نشانگرهای مولکولی. نهال و بذر، 31(1)، 163-187.
دادرضایی، سیدطه؛ افشاری، فرزاد و پاتپور، مهران (1394). ارزیابی فنوتیپی مقاومت به زنگ‌ها در برخی ژنوتیپ‌های گندم ایران در شرایط گلخانه و مزرعه. نهال و بذر، 31(3)، 531-546.
دادرضایی، سیدطه؛ دهقان، محمدعلی؛ صفوی، صفرعلی؛ دالوند، محمد و شهبازی، کمال (1401). بررسی واکنش ژنوتیپ­های پیشرفته و تجاری گندم ایران نسبت به زنگ قهوه­ای در مراحل گیاهچه­ای و گیاه کامل. پژوهش های کاربردی در گیاهپزشکی (دانش کشاورزی)، 11(4)، 1-13.
دادرضائی، سید طه؛ طباطبایی، سید نصرت اله؛ لک زاده، ایرج؛ جعفر نژاد، احمد؛ افشاری، فرزاد و حسن بیات، زهره (1397). ارزیابی تحمل به بیماری‌ زنگ قهوه‌ای در ژنوتیپ‌های منتخب گندم نان. آفات و بیماری‌های گیاهی، 86( 1)، 29-40.
دلفان، صبا؛ بی همتا، محمدرضا؛ دادرضایی، سید طاها؛ عباسی، علیرضا و علیپور، هادی (1400). شناسایی منابع مقاومت به عامل بیماری زنگ قهوه‌ای (Puccinia triticina Eriks.) در ژنوتیپ‌های گندم بومی ایران. دانش گیاهپزشکی ایران، 52(2)، 115-133.
دلفان، صبا؛ بی همتا، محمدرضا؛ دادرضایی، سید طه؛ عباسی، علیرضا و علی پور، هادی (1399). ارزیابی مقاومت به زنگ قهوه‌ای (Puccinia triticina Eriks.) در مرحله گیاهچه‌ای در ژنوتیپ‌های گندم. نهال و بذر، 36(4)، 483-508.
زرندی، فاطمه؛ افشاری، فرزاد و رضائی، سعید (1388). مطالعه اجزاء مقاومت در مرحله گیاهچه‌ای و مقاومت مزرعه‌ای در لاین‌های الیت گندم نسبت به بیماری زنگ قهوه‌ای. نهال و بذر، 25(4)، 569-584.
زرندی، فاطمه؛ افشاری، فرزاد و رضایی، سعید (1390). فاکتورهای بیماری زایی (Puccinia triticina Eriksson) عامل بیماری زنگ قهوه­ای گندم در مناطق مختلف ایران. مجله به نژادی نهال و بذر (نهال و بذر)، 27-1(2)، 219-231.
زهراوی، مهدی؛ دادرضایی، سیدطه و دهقان، محمد علی (1400). غربال ژرم‌پلاسم گندم نان و شناسایی منابع ژنتیکی مقاوم به زنگ قهوه‌ای. تحقیقات غلات، 11(1)، 13-29.
سرهنگی، محسن؛ زینلی­نژاد، خلیل؛ بورنر، آندریاس؛ نصراله­نژاد­قمی، علی­اصغر؛ آقایی­سربرزه، مصطفی؛ دادرضایی، سید­طه و مهرابی، رحیم (1399)  ارزیابی مقاومت به بیماری زنگ قهوه‌ای در ارقام محلی و تجاری گندم نان در شرایط مزرعه و با استفاده از نشانگرهای مولکولی پیوسته به ژن­های Lr34/Yr18/Sr57. نهال و بذر، 36، 271-255.
سعیدمنش، فاطمه؛ نصراله­نژاد­قمی، علی­اصغر؛ زینلی­نژاد، خلیل و کلاته­عربی، مهدی (1393). مطالعه اجزا مقاومت به زنگ قهوه ای در برخی ارقام گندم درمرحله گیاهچه ای. ارایه شده در سیزدهمین همایش علوم زراعت و اصلاح نباتات ایران و سومین همایش علوم و تکنولوژی بذر، کرج، ایران.
شفیعی، آیت­اله؛ ملکی­زنجانی، بهرام؛ کرمی، ثریا و ایمانی­خواه، فرحناز (1389). ردیابی ژن مقاومت به زنگ قهوه ای Lr32در ارقام و لاین های گندم ایرانی با استفاده از آزمون تیپ آلودگی و نشانگرهای مولکولی پیوسته به ژنLr32. پژوهش های تولید گیاهی (علوم کشاورزی و منابع طبیعی)، 17(3)، 21-37.
قاسم زاده، ابراهیم؛ افشاری، فرزاد؛ خدارحمی، منوچهر و بی همتا، محمدرضا (1389). بررسی ژنتیکی مقاومت به بیماری زنگ قهوه­ای در تعدادی از لاین­های پیشرفته گندم در مرحله گیاهچه­ای. زراعت و اصلاح نباتات ایران، 6(3)، 51-59.
کیا، شعبان و افشاری، فرزاد (1390). فاکتورهای بیماریزایی (Puccinia triticina Eriksson) عامل بیماری زنگ قهوه‌ای گندم در استان گلستان در سال‌های 1386-1381. دانش گیاهپزشکی ایران، 42(1)، 51-59.
میرزانیا، مسلم؛ درویش‌نیا، مصطفی؛ احمدی، هادی؛ گودرزی، داریوش و نصرالهی، محمود (1394). مطالعه اجزاء مقاومت در مرحله گیاهچه به بیماری زنگ قهوه‌ای(Puccinia triticina Eriksson) در تعدادی از ارقام تجاری گندم. بیماریهای گیاهی، 51(2)، 263-267.
مهاجروطن، فاطمه؛ نصراله­نژاد­قمی، علی­اصغر؛ کلاته­عربی، مهدی و دهقان، محمدعلی (1393). ارزیابی مقاومت نسبت به بیماری زنگ برگی( قهوه­ای )در برخی از ارقام و لاین­های گندم نان در شرایط مزرعه، مقاله ارایه شده در سیزدهمین همایش علوم زراعت و اصلاح نباتات ایران و سومین همایش علوم و تکنولوژی بذر، کرج، ایران.
مهدیان، صفر علی؛ دهقان، محمد­علی و احمدیان مقدم، محمد­صادق (1383). شناسائی پاتوتیپ های عامل زنگ قهوه ای گندم در استان مازندران و گلستان در سال 1382 . ارایه شده در شانزدهمین کنگره گیاهپزشکی ایران. تبریز، ایران.
نصراله­نژادقمی، علی اصغر؛ حسین­زاده، عبدالهادی؛ ترابی، محمد و قنادها، محمدرضا (1382). بررسی ژنتیکی مقاومت به بیماری زنگ قهوه­ای در تعدادی از لاین­های پیشرفته گندم در مرحله گیاهچه­ای. نهال و بذر، 19(3)، 281-294.
نعمتی، زهرا؛ مستوفی­زاده­قلمفرسا، رضا؛ دادخدایی، علی؛ مهرابی، رحیم و استفنسن، برایان (1397). دامنه‌ی میزبانی جمعیت‌های مختلف زنگ برگی گندم در ایران. بیماریهای گیاهی، 54(4)، 305-316.
نیازمند، علیرضا؛ افشاری، فرزاد؛ عباسی، مهرداد و رضائی، سعید (1389). مطالعه تنوع پاتوتایپ‌ها و فاکتورهای بیماری‌زایی قارچ (Puccinia triticina Eriksson) عامل بیماری زنگ قهوه‌ای گندم در ایران. بیماریهای گیاهی، 46(3)، 187-202.
Afshari, F. (2008, January). Identification of virulence factors of Puccinia triticina, the causal agent of wheat leaf rust in Iran. In Proceedings of 11th international wheat genet symposium (Vol. 3, pp. 709-711).
Afshari, F., Torabi M., Kia, Sh., Dadrezaei, S. T., Safavi, S. A., Chaichi, M., Karbalaei Khiavi, H., Zakeri, A., Bahrami Kamangar, S., Nasrollahi, M., Patpour, M., & Ebrahimnejad, S. (2005). Monitoring of Virulence Factors of Puccinia triticina Eriksson, the Causal Agent of Wheat Leaf Rust in Iran During 2002-2004. Seed and Plant Journal, 21(4), 485-496. (In Persian).
Arzani, A., & Ashraf, M. (2017). Cultivated ancient wheats (Triticum spp.): A potential source of health‐beneficial food products. Comprehensive Reviews in Food Science and Food Safety, 16(3), 477-488.
Ballini, E., Lauter, N., & Wise, R. (2013). Prospects for advancing defense to cereal rusts through genetical genomics. Frontiers in Plant Science, 4, 1-11.
Bamdadian, A., & Houmand, N. (1991, Septemer). Evaluation of 27 wheat cultivars containing resistance genes to leaf rust of wheat (Puccinia recondita) in Ahwaz. In Proceedings of the 10th Plant Protection Congress of Iran, Kerman, Iran. (In Persian).
Bolton, M. D., Kolmer, J. A., & Garvin, D. F. (2008). Wheat leaf rust caused by Puccinia triticina. Molecular plant pathology, 9(5), 563-575.
Caldwell, R. M. (1968, August). Breeding for general and/or specific plant disease resistance. In Proceedings of the Third International Wheat Genetics Symposium, Canberra, Australia. Canberra, Australia.
Cloutier, S., McCallum, B. D., Loutre, C., Banks, T. W., Wicker, T., Feuillet, C., & Jordan, M. C. (2007). Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant molecular biology, 65, 93-106.
Dadrezaei, S. T., & Nazari, K. (2015). Detection of wheat rust resistance genes in some of the Iranian wheat genotypes by molecular markers. Seed and Plant Improvement Journal. 31(1), 163–187. (In Persian).
Dadrezaei, S. T., Dehghan, M. A., Safavi, S. A., Dalvand, M., & Shahbazi, K. (2023). Resistance evaluation of advanced and commercial genotypes of Iranian wheat to leaf rust at seedling and adult plant stages. Journal of applied researches in plant protection, 11(4), 1-13. (In Persian).
Dadrezaei, S. T., Tabatabai, S. N., Lakzadeh, I., Jafar Nejad, A., Afshari, F., & Hassan Bayat, Z. (2017). Evaluation of tolerance to brown rust disease in selected bread wheat genotypes. Plant Pests and Diseases, 86(1), 29-40. (In Persian).
Dadrezaei, S. T., Afshari, F., & Patpour, M. (2014). Phenotypic evaluation of rust resistance in some Iranian wheat genotypes under greenhouse and field conditions. Seed and Plant Improvement Journal 31-1(3), 531-546. (In Persian).
Dakouri, A., McCallum, B. D., Radovanovic, N., & Cloutier, S. (2013). Molecular and phenotypic characterization of seedling and adult plant leaf rust resistance in a world wheat collection. Molecular Breeding, 32, 663-677.
de Sousa, T., Ribeiro, M., Sabença, C., & Igrejas, G. (2021). The 10,000-year success story of wheat!. Foods, 10(9), 2124.
Del Olmo A. I., Rubiales D., & Sillero J. C. (2008). Physiologic specialization of Puccinia triticina in Andalusia (Spain) in 2004 and 2005. In Cereal science and technology for feeding ten billion people: genomics era and beyond. edited by Molina-Cano, J. L., Christou, P., Graner, A., Hammer, K., Jouve, N., Keller, B., Lasa, J. M., Powell, W., Royo, C., Shewry, P., & Stanca, A. M. Zaragoza: CIHEAM / IRTA, 169-171.
Delfan, S., Bihamta, M., Dadrezaei, S. T., Abbasi, A., & Alipour, H. (2022). Identification sources of resistance for leaf rust (Puccinia triticina Erikss.) in Iranian wheat genotypes. Iranian Journal of Plant Protection Science, 52(2), 115-133. (In Persian).
Delfan, S., Bihamta, M.R., Dadrezaei, S. T., Abbasi, A.R., & Aalipour, H. (2020). Evaluation of Resistance to Leaf Rust (Puccinia triticina Eriks.) at Seedling Stage in Wheat Genotypes. Seed and plant Journal. 36(4), 483-508. (In Persian). 
Draz, I. S., Abou-Elseoud, M. S., Kamara, A. E. M., Alaa-Eldein, O. A. E., & El-Bebany, A. F. (2015). Screening of wheat genotypes for leaf rust resistance along with grain yield. Annals of Agricultural sciences, 60(1), 29-39.
Ebrahimian, M., Nasraleh Nejad Qomi, A. A., Zainelinejad, Kh., & Ramzanpour, S. S. (2018). Evaluation of resistance to brown rust in mature plant stage in several bread wheat cultivars. Plant Production Research, 26(3), 89-102. (In Persian).
Esfandiaari, E. (1947). Grain rusts in Iran. Journal of Plant Pests and Diseases, 4. 76-77. (In Persian).
Ghasemzade, E., Afshari. F.M. Khodarahmi and M. Bihamta. 2010. Study on the genetics of resistance to leaf rust in some advanced bread wheat lines at seedling stage. Journal of Agriculture and Breeding, 6, 51-59. (In Persian).
Gultyaeva, E. I., Shaydayuk, E. L., & Kosman, E. G. (2020). Regional and temporal differentiation of virulence phenotypes of Puccinia triticina from common wheat in Russia during the period 2001–2018. Plant pathology, 69(5), 860-871.
Gultyaeva, E., Shaydayuk, E., & Gannibal, P. (2021). Leaf rust resistance genes in wheat cultivars registered in Russia and their influence on adaptation processes in pathogen populations. Agriculture, 11(4), 319.
Hernandez Nopsa, J. F., & Pfender, W. F. (2014). A latent period duration model for wheat stem rust. Plant Disease. 98,1358-1363.
Huang, L., Brooks, S. A., Li, W., Fellers, J. P., Trick, H. N., & Gill, B. S. (2003). Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics, 164(2), 655-664.
Kenzhebayeva, S., Abekova, A., Atabayeva, S., Yernazarova, G., Omirbekova, N., Zhang, G., & Wang, Y. (2019). Mutant lines of spring wheat with increased iron, zinc, and micronutrients in grains and enhanced bioavailability for human health. BioMed Research International. 2019, 1-10.
Kia, Sh., & Afshari, F. (2011). Pathogenic factors of Puccinia triticina Eriksoon, the cause of wheat brown rust disease in Golestan province in 1381-1386. Iranian Journal of Plant Protection Science, 42(1), 51-59. (In Persian).
Kokhmetova, A., Rsaliyev, S., Atishova, M., Kumarbayeva, M., Malysheva, A., Keishilov, Z., & Bolatbekova, A. (2021). Evaluation of wheat germplasm for resistance to leaf rust (Puccinia triticina) and identification of the sources of Lr resistance genes using molecular markers. Plants, 10(7), 1484.
Kolmer, J. A. (2005). Tracking wheat rust on a continental scale. Current Opinion in Plant Biology 8, 441–449.
Kolmer, J. A. (2013). Leaf rust of wheat: pathogen biology, variation and host resistance. Forests, 4(1), 70-84.
Kolmer, J. A., Chao, S., Brown‐Guedira, G., Bansal, U., & Bariana, H. (2018a). Adult plant leaf rust resistance derived from the soft red winter wheat cultivar ‘Caldwell’maps to chromosome 3BS. Crop Science, 58(1), 152-158.
Kolmer, J. A., Su, Z., Bernardo, A., Bai, G., & Chao, S. (2018b). Mapping and characterization of the new adult plant leaf rust resistance gene Lr77 derived from Santa Fe winter wheat. Theoretical and applied genetics, 131, 1553-1560.
Lagudah E. S. (2011). Molecular genetics of race non-specifc resistance in wheat. Euphytica 179:81–91.
Lan, C. X., Singh, R. P., Huerta-Espino, J., Calvo-Salazar, V., & Herrera-Foessel, S. A. (2014). Genetic analysis of resistance to leaf rust and stripe rust in wheat cultivar Francolin# 1. Plant Disease, 98(9), 1227-1234.
Line R. F. (2002). Stripe rust of wheat and barley in North America: A Retrospective Historical Review. Annual Review of Phytopathology 40(1): 75–118.
Mahdian, S. A., Dehghan, M. A., & Ahmadian-Moghadam, M. S. (2004). Identification of wheat leaf rust (Puccinia recondita f. sp. tritici) pathotypes in Mazandaran and Golestan provinces in 2003. In Proceedings of 16th Iran plant protection Congress. Tabriz, Iran. (In Persian).
McIntosh, R., Wellings, C., Park, R. (1995). Wheat Rusts: An Atlas of Resistance Genes. Australia: Csiro Publishing.
Mirzania, M., Darvishnia, M., Ahmadi, H., Ghoudarzi, D., & Nasrolahi, M. (2015). Study of resistance components at seedling stage to leaf rust (Puccinia triticina Eriksson) in some commercial cultivars. Iranian Journal of Plant Pathology, 51(2), 263-267. (In Persian).
Mohajerwatan, F., Nasraleh Nejad Qomi, A. A., Kalate Arabi, M. & Dehghan, M. A. (2013), Evaluation of resistance to leaf rust disease (brown) in some varieties and lines of bread wheat under field conditions, In Proceedings of 13th Agricultural Science and plant breeding Conference of Iran and the third seed science and technology conference. Karaj, Iran. (In Persian).
Nasraleh Nejad Qomi, A. A., Hosseyn Zadeh, A., Torabi, M., & Ghanadha, M. (2003). Study On the Genetics of Resistance to Leaf Rust in Some Advanced Lines of Wheat at Seedling Stage. Seed and Plant Journal, 19(3), 281-294. (In Persian).
Nemati, Z., Mostowfizadeh Ghalamfarsa, R., Dadkhodaie, A., Mehrabi, R., & Steffenson, B. J. (2019). Host range of various leaf rust populations in Iran. Iranian journal of plant pathology, 54(4), 305-316. (In Persian).
Niazmand, A. R., Afshari, F., Abbasi, M., & Rezaee, S. (2010). Study on pathotypes diversity and virulence factors of puccinia triticina eriksson, the causal agent of wheat brown rust in iran. Iranian journal of plant pathology, 46(3), 187-202. (In Persian).
Nopsa, J. F. H., & Pfender, W. F. (2014). A latent period duration model for wheat stem rust. Plant disease, 98(10), 1358-1363.
Peng, F. Y., & Yang, R. C. (2017). Prediction and analysis of three gene families related to leaf rust (Puccinia triticina) resistance in wheat (Triticum aestivum L.). BMC plant biology, 17, 1-17.
Peterson, R. F., Campbell, A. B., & Hannah, A. E. (1948). A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Canadian journal of research, 26(5), 496-500.
Pourkhorshid, Z., Dadkhodaie, A., & Shamloo‐Dashtpagerdi, R. (2022). Molecular analyses in wheat and Aegilops tauschii reveal a new orthologue of the leaf rust resistance gene Lr19 on chromosome 7DL of Ae. tauschii. Journal of Phytopathology, 170(4), 255-263.
Quan, W., Hou, G., Chen, J., Du, Z., Lin, F., Guo, Y., & Zhang, Z. (2013). Mapping of QTL lengthening the latent period of Puccinia striiformis in winter wheat at the tillering growth stage. European journal of plant pathology, 136, 715-727.
Rafiei, F., Arzani, A., Afshari, F., & Torabi, M. (2007). Characterization of leaf rust resistance genes in seedlings of wheat cultivars. Genetic and Breeding, 36, 19-27. (In Persian).
Ren, X., Wang, C., Ren, Z., Wang, J., Zhang, P., Zhao, S., & Wang, X. (2023). Genetics of resistance to leaf rust in wheat: an overview in a genome-wide level. Sustainability, 15(4), 3247.
Roelfs A.P., Singh R.P., Saari E.E. (1992) Rust diseases of wheat: concepts and methods of disease management. CIMMYT, Mexico.
Saeedmanesh, F., Nasraleh Nejad Qomi, A. A., Zainlinejad, K., & Kalatearabi, M. (2013). Studying the components of resistance to brown rust in some wheat cultivars at the seedling stage. 13Iranian Crop Sciences Congress & 3rd Iranian Seed Science and Technology Conference. Karaj, Iran. (In Persian).
Sarhangi, M., Zaynali Nezhad, K., Börner, A., Nasrollahnezhad Qomi. A., Aghaee Sarbarzeh, A., Dadrezaei, S. T., & Mehrabi, R. (2020). Evaluation of Resistance to Leaf Rust in Bread Wheat Landraces and Commercial Cultivars Under Field Conditions and By Using Molecular Markers Linked to Lr34/Yr18/Sr57 Genes M. Seed and Plant Journal, 36(3), 255-271. (In Persian).
Shafie, A., Maleki Zanjani, B., Karami S., & Imani Khah F. (2012). Detection of leaf rust resistance gene Lr32 in Iranian wheat varieties and lines using infection-type data test and molecular markers linked to the Lr32. Journal of Plant Production Research. 17(3), 21-37.
Shaner, G. (1980). Probits for analyzing latent period data in studies of slow rusting resistance. Phytopathology, 70(12), 1179-82.
Singh, D., Simmonds, J., Park, R. F., Bariana, H. S., & Snape, J. W. (2009). Inheritance and QTL mapping of leaf rust resistance in the European winter wheat cultivar ‘Beaver’. Euphytica, 169, 253-261.
Singh, J., Gudi, S., Maughan, P. J., Liu, Z., Kolmer, J., Wang, M., & Gill, U. (2024). Genomes of Aegilops umbellulata provide new insights into unique structural variations and genetic diversity in the U-genome for wheat improvement. bioRxiv, 2024-01.
Singh, R. P., Huerta-Espino, J., Pfeiffer, W., & Figueroa-Lopez, P. (2004). Occurrence and impact of a new leaf rust race on durum wheat in northwestern Mexico from 2001 to 2003. Plant disease, 88(7), 703-708.
Singh, R.P., Huerta-Espino, J. and Rajaram, S. (2000) Achieving nearimmunity to leaf rust and stripe rust in wheat by combining slow rusting resistance genes. Acta Phytopathologica et Entomologica Hungarica. 35, 133–139.
Torabi, M., Nazari, K., & Afshari, F. (2002). Genetics of pathogenicity of Puccinia recondita f. sp. tritici, the causal agent of leaf rust of wheat. Iranian Journal of Agricultural Science, 32, 625-635. (In Persian).
Tripathi, A. D., Mishra, R., Maurya, K. K., Singh, R. B., & Wilson, D. W. (2019). Estimates for world population and global food availability for global health. In The role of functional food security in global health. Academic Press. (pp. 3-24).
Vale, F. X. R., Parlevliet, J. E., & Zambolim, L. (2001). Concepts in plant disease resistance. Fitopatologia Brasileira, 26, 577-589.
Winter, G. (1884). Rabenhorstii Fungi europaei et extraeuropaei exsiccati cura Dr. G. Winter, Centuria XXXI et XXXII. Hedwigia, 23, 164-172.
Xiao, D., Li Liu, D., Wang, B., Feng, P., Bai, H., & Tang, J. (2020). Climate change impact on yields and water use of wheat and maize in the North China Plain under future climate change scenarios. Agricultural Water Management, 238, 106238.
Yang, F., Zhang, J., Liu, Q., Liu, H., Zhou, Y., Yang, W., & Ma, W. (2022). Improvement and Re-Evolution of Tetraploid Wheat for Global Environmental Challenge and Diversity Consumption Demand. International Journal of Molecular Sciences, 23(4), 2206
Zahravi, M., Dadrezaei, S. T., & Dehghan, M. A. (2021). Screening of bread wheat germplasm and identification of genetic resources resistant to leaf rust disease. Cereal Research, 11(1), 13-29. (In Persian).
Zarandi, F., Afshari, F., & Rezaei, S. (2009). Study of Resistance Components at Seedling Stage and Field Resistance to Leaf Rust in some Elite Wheat Lines. Seed and Plant Journal, 25(4), 569-584. (In Persian).
Zhang, D., Bowden, R. L., Yu, J., Carver, B. F., & Bai, G. (2014). Association analysis of stem rust resistance in US winter wheat. PLoS One, 9(7), e103747.
Zhang, L., Zhao, X., Liu, J., Wang, X., Gong, W., Zhang, Q., & Liu, D. (2022). Evaluation of the resistance to Chinese predominant races of Puccinia triticina and analysis of effective leaf rust resistance genes in wheat accessions from the US National Plant Germplasm System. Frontiers in Plant Science, 13, 1054673.